Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer's disease-related pathologies in male triple-transgenic mice

BMC Neuroscience

Volumn 9, Issue , 2008, Pages

  Mastrangelo, Michael A ^a   Bowers, William J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN REGION; CELL ACTIVATION; CONTROLLED STUDY; DISEASE COURSE; ENTORHINAL CORTEX; GENE ACTIVITY; GENE FUNCTION; GENE OVEREXPRESSION; HIPPOCAMPUS; IMMUNOPATHOLOGY; MALE; MICROGLIA; MOTOR CORTEX; MOUSE; NERVE FIBER TRANSPORT; NONHUMAN; ONSET AGE; PAIRED HELICAL FILAMENT; PLAQUE FORMING CELL; PYRAMIDAL NERVE CELL; TRANSGENE; TRANSGENIC MOUSE; AGE; ANIMAL; BRAIN; BRAIN LEVEL; CHEMISTRY; COMPARATIVE STUDY; DISEASE MODEL; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; NEUROFIBRILLARY TANGLE; PATHOLOGY; PHYSIOLOGY; SENILE PLAQUE;

AGE FACTORS; ALZHEIMER DISEASE; ANIMALS; BRAIN; BRAIN CHEMISTRY; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; NEUROFIBRILLARY TANGLES; SENILE PLAQUES;

EID: 51049120310     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-9-81     Document Type: Article

References (75)

1. Ferri CP Prince M Brayne C Brodaty H Fratiglioni L Ganguli M Hall K Hasegawa K Hendrie H Huang Y Jorm A Mathers C Menezes PR Rimmer E Scazufca M Global prevalence of dementia: A Delphi consensus study Lancet 2005, 366(9503):2112-2117. 10.1016/S0140-6736(05)67889-0 16360788
2. Atwood CS Martins RN Smith MA Perry G Senile plaque composition and posttranslational modification of amyloid-beta peptide and associated proteins Peptides 2002, 23(7):1343-1350. 10.1016/S0196-9781(02)00070-0 12128091
3. Braak H Braak E Frequency of stages of Alzheimer-related lesions in different age categories Neurobiol Aging 1997, 18(4):351-357. 10.1016/ S0197-4580(97)00056-0 9330961
4. Hsiao K Chapman P Nilsen S Eckman C Harigaya Y Younkin S Yang F Cole G Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice Science 1996, 274(5284):99-102. 10.1126/ science.274.5284.99 8810256
5. Oster-Granite ML McPhie DL Greenan J Neve RL Age-dependent neuronal and synaptic degeneration in mice transgenic for the C terminus of the amyloid precursor protein J Neurosci 1996, 16(21):6732-6741. 8824314
6. Neve RL Boyce FM McPhie DL Greenan J Oster-Granite ML Transgenic mice expressing APP-C100 in the brain Neurobiol Aging 1996, 17(2):191-203. 10.1016/0197-4580(95)02074-8 8744400
7. Moechars D Dewachter I Lorent K Reverse D Baekelandt V Naidu A Tesseur I Spittaels K Haute CV Checler F Godaux E Cordell B Van Leuven F Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain J Biol Chem 1999, 274(10):6483-6492. 10.1074/jbc.274.10.6483 10037741
8. Sturchler-Pierrat C Abramowski D Duke M Wiederhold KH Mistl C Rothacher S Ledermann B Burki K Frey P Paganetti PA Waridel C Calhoun ME Jucker M Probst A Staufenbiel M Sommer B Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology Proc Natl Acad Sci U S A 1997, 94(24):13287-13292. 24301 9371838 10.1073/pnas.94.24.13287
9. Games D Adams D Alessandrini R Barbour R Berthelette P Blackwell C Carr T Clemens J Donaldson T Gillespie F et al.: Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein Nature 1995, 373(6514):523-527. 10.1038/373523a0 7845465
10. Bronfman FC Moechars D Van Leuven F Acetylcholinesterase-positive fiber deafferentation and cell shrinkage in the septohippocampal pathway of aged amyloid precursor protein london mutant transgenic mice Neurobiol Dis 2000, 7(3):152-168. 10.1006/nbdi.2000.0283 10860782
11. Boutajangout A Leroy K Touchet N Authelet M Blanchard V Tremp G Pradier L Brion JP Increased tau phosphorylation but absence of formation of neurofibrillary tangles in mice double transgenic for human tau and Alzheimer mutant (M146L) presenilin-1 Neurosci Lett 2002, 318(1):29-33. 10.1016/S0304-3940(01)02461-2 11786218
12. Gotz J Chen F Barmettler R Nitsch RM Tau filament formation in transgenic mice expressing P301L tau J Biol Chem 2001, 276(1):529-534. 10.1074/jbc.M006531200 11013246
13. Ishihara T Hong M Zhang B Nakagawa Y Lee MK Trojanowski JQ Lee VM Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform Neuron 1999, 24(3):751-762. 10.1016/S0896-6273(00)81127-7 10595524
14. Probst A Gotz J Wiederhold KH Tolnay M Mistl C Jaton AL Hong M Ishihara T Lee VM Trojanowski JQ Jakes R Crowther RA Spillantini MG Burki K Goedert M Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein Acta Neuropathol (Berl) 2000, 99(5):469-481. 10.1007/s004010051148
15. Spittaels K Van den Haute C Van Dorpe J Bruynseels K Vandezande K Laenen I Geerts H Mercken M Sciot R Van Lommel A Loos R Van Leuven F Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein Am J Pathol 1999, 155(6):2153-2165. 1866931 10595944
16. Tanemura K Akagi T Murayama M Kikuchi N Murayama O Hashikawa T Yoshiike Y Park JM Matsuda K Nakao S Sun X Sato S Yamaguchi H Takashima A Formation of filamentous tau aggregations in transgenic mice expressing V337M human tau Neurobiol Dis 2001, 8(6):1036-1045. 10.1006/ nbdi.2001.0439 11741399
17. Oddo S Caccamo A Shepherd JD Murphy MP Golde TE Kayed R Metherate R Mattson MP Akbari Y LaFerla FM Triple-transgenic model of Alzheimer's disease with plaques and tangles: Intracellular Abeta and synaptic dysfunction Neuron 2003, 39(3):409-421. 10.1016/S0896-6273(03)00434-3 12895417
18. Oddo S Caccamo A Kitazawa M Tseng BP LaFerla FM Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease Neurobiol Aging 2003, 24(8):1063-1070. 10.1016/ j.neurobiolaging.2003.08.012 14643377
19. Billings LM Oddo S Green KN McGaugh JL LaFerla FM Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice Neuron 2005, 45(5):675-688. 10.1016/ j.neuron.2005.01.040 15748844
20. Haass C Lemere CA Capell A Citron M Seubert P Schenk D Lannfelt L Selkoe DJ The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway Nat Med 1995, 1(12):1291-1296. 10.1038/nm1295-1291 7489411
21. Duff K Eckman C Zehr C Yu X Prada CM Perez-tur J Hutton M Buee L Harigaya Y Yager D Morgan D Gordon MN Holcomb L Refolo L Zenk B Hardy J Younkin S Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1 Nature 1996, 383(6602):710-713. 10.1038/383710a0 8878479
22. Borchelt DR Thinakaran G Eckman CB Lee MK Davenport F Ratovitsky T Prada CM Kim G Seekins S Yager D Slunt HH Wang R Seeger M Levey AI Gandy SE Copeland NG Jenkins NA Price DL Younkin SG Sisodia SS Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo Neuron 1996, 17(5):1005-1013. 10.1016/ S0896-6273(00)80230-5 8938131
23. Nunan J Small DH Regulation of APP cleavage by alpha-, beta- and gamma-secretases FEBS Lett 2000, 483(1):6-10. 10.1016/ S0014-5793(00)02076-7 11033346
24. Caroni P Overexpression of growth-associated proteins in the neurons of adult transgenic mice J Neurosci Methods 1997, 71(1):3-9. 10.1016/ S0165-0270(96)00121-5 9125370
25. LaFerla FM Green KN Oddo S Intracellular amyloid-beta in Alzheimer's disease Nat Rev Neurosci 2007, 8(7):499-509. 10.1038/nrn2168 17551515
26. Oddo S Caccamo A Smith IF Green KN LaFerla FM A dynamic relationship between intracellular and extracellular pools of Abeta Am J Pathol 2006, 168(1):184-194. 1592652 16400022 10.2353/ajpath.2006.050593
27. D'Andrea MR Reiser PA Polkovitch DA Gumula NA Branchide B Hertzog BM Schmidheiser D Belkowski S Gastard MC Andrade-Gordon P The use of formic acid to embellish amyloid plaque detection in Alzheimer's disease tissues misguides key observations Neurosci Lett 2003, 342(1-2):114-118. 10.1016/S0304-3940(03)00252-0 12727331
28. Ohyagi Y Tsuruta Y Motomura K Miyoshi K Kikuchi H Iwaki T Taniwaki T Kira J Intraneuronal amyloid beta42 enhanced by heating but counteracted by formic acid J Neurosci Methods 2007, 159(1):134-138. 10.1016/ j.jneumeth.2006.06.010 16860394
29. Cleveland DW Hwo SY Kirschner MW Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin J Mol Biol 1977, 116(2):207-225. 10.1016/ 0022-2836(77)90213-3 599557
30. Wijker M Wszolek ZK Wolters EC Rooimans MA Pals G Pfeiffer RF Lynch T Rodnitzky RL Wilhelmsen KC Arwert F Localization of the gene for rapidly progressive autosomal dominant parkinsonism and dementia with pallido-ponto-nigral degeneration to chromosome 17q21 Hum Mol Genet 1996, 5(1):151-154. 10.1093/hmg/5.1.151 8789453
31. Sahara N Lewis J DeTure M McGowan E Dickson DW Hutton M Yen SH Assembly of tau in transgenic animals expressing P301L tau: Alteration of phosphorylation and solubility J Neurochem 2002, 83(6):1498-1508. 10.1046/j.1471-4159.2002.01241.x 12472903
32. Gustke N Trinczek B Biernat J Mandelkow EM Mandelkow E Domains of tau protein and interactions with microtubules Biochemistry 1994, 33(32):9511-9522. 10.1021/bi00198a017 8068626
33. Kosik KS McConlogue L Microtubule-associated protein function: Lessons from expression in Spodoptera frugiperda cells Cell Motil Cytoskeleton 1994, 28(3):195-198. 10.1002/cm.970280302 7954847
34. Drubin DG Kirschner MW Tau protein function in living cells J Cell Biol 1986, 103(6 Pt 2):2739-2746. 2114585 3098742 10.1083/jcb.103.6.2739
35. Weingarten MD Lockwood AH Hwo SY Kirschner MW A protein factor essential for microtubule assembly Proc Natl Acad Sci U S A 1975, 72(5):1858-1862. 432646 1057175 10.1073/pnas.72.5.1858
36. Goedert M Wischik CM Crowther RA Walker JE Klug A Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: Identification as the microtubule-associated protein tau Proc Natl Acad Sci U S A 1988, 85(11):4051-4055. 280359 3131773 10.1073/pnas.85.11.4051
37. Ksiezak-Reding H Morgan K Mattiace LA Davies P Liu WK Yen SH Weidenheim K Dickson DW Ultrastructure and biochemical composition of paired helical filaments in corticobasal degeneration Am J Pathol 1994, 145(6):1496-1508. 1887493 7992852
38. Kosik KS Orecchio LD Binder L Trojanowski JQ Lee VM Lee G Epitopes that span the tau molecule are shared with paired helical filaments Neuron 1988, 1(9):817-825. 10.1016/0896-6273(88)90129-8 2483104
39. Greenberg SG Davies P A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis Proc Natl Acad Sci U S A 1990, 87(15):5827-5831. 54421 2116006 10.1073/pnas.87.15.5827
40. Papasozomenos SC Tau protein immunoreactivity in dementia of the Alzheimer type: II. Electron microscopy and pathogenetic implications. Effects of fixation on the morphology of the Alzheimer's abnormal filaments Lab Invest 1989, 60(3):375-389. 2494388
41. Trojanowski JQ Lee VMY Transgenic models of tauopathies and synucleinopathies Brain Pathology 1999, 9:733-739. 10517511
42. Grundke-Iqbal I Iqbal K Tung YC Quinlan M Wisniewski HM Binder LI Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology Proc Natl Acad Sci U S A 1986, 83(13):4913-4917. 323854 3088567 10.1073/pnas.83.13.4913
43. Bancher C Brunner C Lassmann H Budka H Jellinger K Wiche G Seitelberger F Grundke-Iqbal I Iqbal K Wisniewski HM Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease Brain Res 1989, 477(1-2):90-99. 10.1016/ 0006-8993(89)91396-6 2495152
44. Wischik CM Edwards PC Lai RY Gertz HN Xuereb JH Paykel ES Brayne C Huppert FA Mukaetova-Ladinska EB Mena R et al.: Quantitative analysis of tau protein in paired helical filament preparations: Implications for the role of tau protein phosphorylation in PHF assembly in Alzheimer's disease Neurobiol Aging 1995, 16(3):409-17; discussion 418-31. 10.1016/ 0197-4580(95)97327-D 7566350
45. Mandelkow EM Biernat J Drewes G Gustke N Trinczek B Mandelkow E Tau domains, phosphorylation, and interactions with microtubules Neurobiol Aging 1995, 16(3):355-62; discussion 362-3. 10.1016/0197-4580(95)00025-A 7566345
46. Biernat J Gustke N Drewes G Mandelkow EM Mandelkow E Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: Distinction between PHF-like immunoreactivity and microtubule binding Neuron 1993, 11(1):153-163. 10.1016/0896-6273(93)90279-Z 8393323
47. Lee VM Goedert M Trojanowski JQ Neurodegenerative tauopathies Annu Rev Neurosci 2001, 24:1121-1159. 10.1146/annurev.neuro.24.1.1121 11520930
48. Vega IE Cui L Propst JA Hutton ML Lee G Yen SH Increase in tau tyrosine phosphorylation correlates with the formation of tau aggregates Brain Res Mol Brain Res 2005, 138(2):135-144. 10.1016/ j.molbrainres.2005.04.015 15913839
49. Oddo S Caccamo A Cheng D Jouleh B Torp R LaFerla FM Genetically augmenting tau levels does not modulate the onset or progression of Abeta pathology in transgenic mice J Neurochem 2007, 102(4):1053-1063. 10.1111/j.1471-4159.2007.04607.x 17472708
50. Alonso A Zaidi T Novak M Grundke-Iqbal I Iqbal K Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/ straight filaments Proc Natl Acad Sci U S A 2001, 98(12):6923-6928. 34454 11381127 10.1073/pnas.121119298
51. Vincent I Rosado M Kim E Davies P Increased production of paired helical filament epitopes in a cell culture system reduces the turnover of tau J Neurochem 1994, 62(2):715-723. 507514
52. Janelsins MC Mastrangelo MA Oddo S LaFerla FM Federoff HJ Bowers WJ Early correlation of microglial activation with enhanced tumor necrosis factor-alpha and monocyte chemoattractant protein-1 expression specifically within the entorhinal cortex of triple transgenic Alzheimer's disease mice J Neuroinflammation 2005, 2:23. 1276812 16232318 10.1186/1742-2094-2-23
53. D'Andrea MR Cole GM Ard MD The microglial phagocytic role with specific plaque types in the Alzheimer disease brain Neurobiol Aging 2004, 25(5):675-683. 10.1016/j.neurobiolaging.2003.12.026 15172747
54. Eikelenboom P Veerhuis R Scheper W Rozemuller AJ van Gool WA Hoozemans JJ The significance of neuroinflammation in understanding Alzheimer's disease J Neural Transm 2006, 113(11):1685-1695. 10.1007/ s00702-006-0575-6 17036175
55. Gahtan E Overmier JB Inflammatory pathogenesis in Alzheimer's disease: biological mechanisms and cognitive sequeli Neurosci Biobehav Rev 1999, 23(5):615-633. 10.1016/S0149-7634(98)00058-X 10392655
56. Cotrina ML Nedergaard M Astrocytes in the aging brain J Neurosci Res 2002, 67(1):1-10. 10.1002/jnr.10121 11754075
57. Heneka MT Wiesinger H Dumitrescu-Ozimek L Riederer P Feinstein DL Klockgether T Neuronal and glial coexpression of argininosuccinate synthetase and inducible nitric oxide synthase in Alzheimer disease J Neuropathol Exp Neurol 2001, 60(9):906-916. 11556547
58. Skaper SD Facci L Leon A Inflammatory mediator stimulation of astrocytes and meningeal fibroblasts induces neuronal degeneration via the nitridergic pathway J Neurochem 1995, 64(1):266-276. 7798922
59. Sheetz MP Pfister KK Bulinski JC Cotman CW Mechanisms of trafficking in axons and dendrites: Implications for development and neurodegeneration Prog Neurobiol 1998, 55(6):577-594. 10.1016/S0301-0082(98)00021-5 9670219
60. van Groen T Miettinen P Kadish I The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation Hippocampus 2003, 13(1):133-149. 10.1002/hipo.10037 12625464
61. Witter MP Connectivity of the rat hippocampus. The Hippocampus-New Vistas Hoboken, Wiley, John & Sons, Inc. Chan-Palay VE 1989:53-69.
62. Glabe C Intracellular mechanisms of amyloid accumulation and pathogenesis in Alzheimer's disease J Mol Neurosci 2001, 17(2):137-145. 10.1385/JMN:17:2:137 11816787
63. Nagele RG Wegiel J Venkataraman V Imaki H Wang KC Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease Neurobiol Aging 2004, 25(5):663-674. 10.1016/ j.neurobiolaging.2004.01.007 15172746
64. Cummings BJ Su JH Geddes JW Van Nostrand WE Wagner SL Cunningham DD Cotman CW Aggregation of the amyloid precursor protein within degenerating neurons and dystrophic neurites in Alzheimer's disease Neuroscience 1992, 48(4):763-777. 10.1016/0306-4522(92)90265-4 1378573
65. Irizarry MC Soriano F McNamara M Page KJ Schenk D Games D Hyman BT Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse J Neurosci 1997, 17(18):7053-7059. 9278541
66. Eriksen JL Janus CG Plaques, tangles, and memory loss in mouse models of neurodegeneration Behav Genet 2007, 37(1):79-100. 10.1007/ s10519-006-9118-z 17072762
67. Callahan MJ Lipinski WJ Bian F Durham RA Pack A Walker LC Augmented senile plaque load in aged female beta-amyloid precursor protein-transgenic mice Am J Pathol 2001, 158(3):1173-1177. 1850367 11238065
68. Clinton LK Billings LM Green KN Caccamo A Ngo J Oddo S McGaugh JL LaFerla FM Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice Neurobiol Dis 2007, 28(1):76-82. 10.1016/ j.nbd.2007.06.013 17659878
69. Carroll JC Rosario ER Chang L Stanczyk FZ Oddo S LaFerla FM Pike CJ Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice J Neurosci 2007, 27(48):13357-13365. 10.1523/ JNEUROSCI.2718-07.2007 18045930
70. Gotz J Chen F van Dorpe J Nitsch RM Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils Science 2001, 293(5534):1491-1495. 10.1126/science.1062097 11520988
71. Hock C Konietzko U Papassotiropoulos A Wollmer A Streffer J von Rotz RC Davey G Moritz E Nitsch RM Generation of antibodies specific for beta-amyloid by vaccination of patients with Alzheimer disease Nat Med 2002, 8(11):1270-1275. 10.1038/nm783 12379846
72. Oddo S Caccamo A Green KN Liang K Tran L Chen Y Leslie FM LaFerla FM Chronic nicotine administration exacerbates tau pathology in a transgenic model of Alzheimer's disease Proc Natl Acad Sci U S A 2005, 102(8):3046-3051. 549455 15705720 10.1073/pnas.0408500102
73. Parvathy S Davies P Haroutunian V Purohit DP Davis KL Mohs RC Park H Moran TM Chan JY Buxbaum JD Correlation between Abetax-40-, Abetax-42-, and Abetax-43-containing amyloid plaques and cognitive decline Arch Neurol 2001, 58(12):2025-2032. 10.1001/archneur.58.12.2025 11735776
74. Mercken M Vandermeeren M Lubke U Six J Boons J Vanmechelen E Van de Voorde A Gheuens J Affinity purification of human tau proteins and the construction of a sensitive sandwich enzyme-linked immunosorbent assay for human tau detection J Neurochem 1992, 58(2):548-553. 10.1111/ j.1471-4159.1992.tb09754.x 1729400
75. Shaftel SS Kyrkanides S Olschowka JA Miller JN Johnson RE O'Banion MK Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology J Clin Invest 2007, 117(6):1595-1604. 1878531 17549256 10.1172/JCI31450